Rev. bras. farmacogn. vol.18 número1

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Revisão

Sources of alpha-, beta-, gamma-, delta- and epsilon-carotenes:

A twentieth century review

**José M. Barbosa-Filho,* Adriana A. Alencar, Xirley P. Nunes, Anna C. de Andrade Tomaz,**

José G. Sena-Filho, Petrônio F. Athayde-Filho, Marcelo S. Silva, Maria F. Vanderlei de

Souza, Emidio V. Leitão da-Cunha

Laboratório de Tecnologia Farmacêutica, Universidade Federal da Paraíba, Caixa Postal 5009,

58051-970 João Pessoa-PB, Brazil

RESUMO: “Fontes de alfa-, beta-, gama-, delta-, e epsilon-carotenos: Uma revisão do século XX”.Uma vez que os humanos não podem sintetizar carotenóides, dependem exclusivamente da dieta como fonte desses micronutrientes. Tem sido aﬁ rmado que eles podem aliviar doenças crônicas, tais como cânceres. O presente artigo constitui uma revisão global da literatura cientíﬁ ca sobre plantas e outros organismos que biossintetizam carotenóides, que incluem as séries alfa-, beta-, gama-, delta-, e epsilon-carotenos. Os resultados das listas de pesquisa da literatura mostram mais de quinhentas fontes.

Unitermos: D-Caroteno,E-caroteno,J-caroteno,G-caroteno,H-caroteno, carotenóides, câncer, revisão.

ABSTRACT: Since humans cannot synthesize carotenoids, they depend upon the diet exclusively for the source of these micronutrients. It has claimed that they may alleviate chronic diseases such as cancers. The present communication constitutes a global review of the scientiﬁ c literature on plants and others organisms that biosynthesize carotenoids, which include the series alpha-, beta-, gamma-, delta- and epsilon-carotenes. The results of the literature survey lists more than

ﬁ ve hundred sources.

Keywords: D-Carotene, E-carotene, J-carotene, G-carotene, H-carotene, carotenoids, cancer, review.

INTRODUCTION

The carotenoids constitute the largest class

of naturally occurring pigments and have attracted the

attention of chemists and biologists since 1831, when

an yellow coloring agent named

E

-carotene was isolated

from the carrot (

Daucus carota

) for the

ﬁ

rst time. Many

treatises have been devoted to the almost 1000

cis-trans

carotenoid isomers characterized in nature (Britton,

1984, 1985, 1986, 1989, 1991). Most have 40 carbon

atoms, less than 10% are hydrocarbons, most have

oxygen functions, and some are conjugated with sugars

and other molecules. Major provitamin A in mammals

are

E

-carotene and

D

-carotene, although

J

-carotene and

approximately 50 other carotenoids also show some

nutritional activity. Carotenoids are synthesized in plants

from acetyl-coenzyme A by a series of well-de

ﬁ

ned

condensations reactions. The synthesis of carotenoids

does not occur in animal tissue; however, when those

pigments are ingested in the diet, the animals deposit or

modify their basic structure (Olson, 1989).

Most cancers that are common nowadays are

not caused by the products of modern industry, but by

the lifestyle, especially the diet. The scienti

ﬁ

c literature

is consistent in evidences that it is possible to reduce

the risk of acquiring some types of cancer by eating a

variety of vegetables and fruits (Steinmetz & Potter,

1996; Federmann & Federmann, 2000). The types of

vegetable or fruit that most often appear to be protective

against cancer are raw vegetables, followed by allium,

carrots, green vegetables, cruciferous vegetables,

and tomatoes. Substances present in vegetables and

fruit that may help protect against cancer, and their

mechanisms, include, allium compounds,

ﬂ

avonoids,

protease inhibitors, saponins, phytosterols, carotenoids,

vitamins, selenium and dietary

ﬁ

ber. Increment in

vegetable and fruit consumption, include also bene

ﬁ

ts

against cardiovascular disease, diabetes, stroke, obesity,

diverticulosis, and cataracts (Peto et al., 1981).

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prevention of osteoporosis (Pereira et al., 2002), for the

treatment of Parkinson’s disease (Morais et al., 2003),

with antileishmanial (Rocha et al., 2005), hypoglycemic

(Barbosa-Filho et al., 2005), antiin

ﬂ

ammatory activity

(Falcão et al., 2005, Barbosa-Filho et al., 2006a),

inhibitors of the enzyme acetylcholinesterase

(Barbosa-Filho et al., 2006b), inhibitors of the angiotensin

converting enzymes (Barbosa-Filho et al., 2006c),

giardicidal (Amaral et al., 2006), and antileprotic

activity (Barbosa-Filho et al., 2007).

This work aims at presenting the main natural

sources of carotenoids, which include the series

D

-,

E

-,

J

- ,

G

- and

H

-carotene.

MATERIAL AND METHODS

An extensive literature search was carried out

using the Chemical Abstract, Biological Abstract and in

the data bank of the University of Illinois in Chicago

- NAPRALERT (Acronym for NAtural PRoducts

ALERT), updated to March 2000.

The keywords used (in various combinations)

in the search were: plants natural products, carotenoids,

alpha-, beta-, gamma-, delta- and epsilon-carotene. The

references found in the search were then consulted.

Consultation of various types of literature

resulted in the elaboration of a list of occurrence of

alpha-, beta-, gamma-, delta- and epsilon-carotene in

plants and other organisms. For details the original

references should be consulted.

Source of carotenoids

Carotenoids are found almost everywhere in

nature, but particularly among organisms that bask in

the sun. Those interesting compounds, most of which

show a yellow to red color, have attracted the attention

of chemists and biologists since at least the early 1800s.

The colored compounds in plants and microorganisms

were extracted and puri

ﬁ

ed, and in time their structures

were determined. Many treatises have been devoted to

these compounds (Isler, 1971) the most comprehensive

revision were presented by Briton (Britton, 1984, 1985,

1986, 1989, 1991).

We encountered 690 carotenes reported in the

literature, 477 are found to be

E

-carotene, 144

D

-carotene,

43 J

-carotene, 22

H

-carotene and 4

G

-carotene, so 310 are

found in Dicotyledons, 122 Monocotyledons, 76 algae,

44 Gymnosperms, 22 ferns and allies, 8 lichens, 5 fungi,

4 bacteria and 2 insects.

Orange vegetables, such as carrots, sweet

potatoes, winter squash, and pumpkin, are relatively

rich sources of

E

-carotene, as are some fruits, including

papaya, mango and cantaloupe. Because of the interest

of carotenoids in preventing many types of cancer, it

is also important to know which speci

ﬁ

c plants keep

the greatest number of them. We found that

Calendula

arvensis, C. of

ﬁ

cinalis, Citrus paradise, Daucus carota

and

Diospiros kaki

biosynthesize

D

-,

E

-,

J

-

G

- and

H

-carotenes (Table 1).

H

α-Carotene

β-Carotene

γ-Carotene

H

δ-Carotene

ε-Carotene

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Acanthopanax sp Araliaceae D √ Zorikov & Burii, 1974 Acanthophora spicifera Rhodomelaceae D √ Aihara & Yamamoto, 1968 Acidum aculeatum Aspleniaceae FE √ √ Czeczuga, 1985b Acidum angulare Aspleniaceae FE √ √ Czeczuga, 1985b Adiantum capillus-veneris Pteridaceae FE √ √ Czeczuga, 1985b Adiantum pedatum Pteridaceae FE √ Czeczuga, 1985b Adiantum venustum Pteridaceae FE √ √ Czeczuga, 1985b Aesculus hippocastanum Hippocastanaceae D √ Souleles & Vayas, 1986 Agastache foeniculum Lamiaceae D √ Menghini et al.,1992

Aglais urticae Nymphalidae I √ Kayser, 1975

Alectoria nigricans Parmeliaceae L √ √ Czeczuga & Olech, 1990

Allium cepa Liliaceae M √ Granado, 1992

Aloe vera Liliaceae M √ Rowe & Parks, 1941 Amaranthus tricolor Amaranthaceae D √ Rao, 1967 Amblystegium riparium Amblystegiaceae FE √ √ Czeczuga, 1980a Anabaena hallensis Nostocaceae A √ Hai et al., 1996 Anacystis nidulans Chroococcaceae A √ Buchecker et al., 1976

Ananas comosus Bromeliaceae M √ √ Morgan,1966

Aneura pinguis Aneuraceae FE √ Benesova, 1969

Angelica tatianae Apiaceae D √ Aprikyan, 1979

Anisomorpha buprestoides Bacunculidae I √ Davidson, 1991 Ankistrodesmus braunii Oocystaceae A √ Burczyk, 1987 Anthurus archeri Clathraceae FU √ Czygan, 1975

Aphanizomenon flos-aquae Nostocaceae A √ Hertzberg & Jensen, 1966 Apium graveolens Apiaceae D √ Fraczek et al., 1977 Gupta et al., 1980 Aplysia fasciata Aplysiidae S √ Czeczuga, 1984

Aplysia rosea Aplysiidae S √ √ Czeczuga, 1984

Arabidopsis thaliana Brassicaceae D √ Parry & Horgan, 1992 Argania spinosa Sapotaceae D √ Collier &Lemaire, 1974 Arnica montana Asteraceae D √ √ Vanhaelen, 1973 Aronia melanocarpa Rosaceae D √ Razungles et al., 1989 Artemisia dracunculus Asteraceae D √ Prodan et al., 1973

Trofimova, 1977 Artemisia sylvatica Asteraceae D √ Moon et al., 1999 Arum maculatum Araceae M √ Valadon & Mummery, 1975 Ascidia zara Ascidiidae S √ Ookubo & Matsuno, 1985 Ascophyllum nodosum Fucaceae A √ Haugan & Jensen, 1994 Asparagus officinalis Liliaceae M √ √ Simpson et al., 1977

Bureau & Bushway, 1986 Granado et al., 1992

Aspidium lobatum Dryopteridaceae FE √ √ Czeczuga, 1985b Asplenium lanceolatum Aspleniaceae FE √ √ Czeczuga, 1985b Asplenium trichomanes Aspleniaceae FE √ Czeczuga, 1985b Asterias amurensis Asteriidae S √ Maoka et al., 1989 Asterina pectinifera Asterinidae S √ Maoka et al., 1989 Athyrium filix- femina Dryopteridaceae FE √ Czeczuga, 1985b Averrhoa carambola Oxalidaceae D √ √ Gross, 1983

Basella alba Basellaceae D √ Cyunel & Czygan, 1989 Berberis amurensis Berberidaceae D √ Shapiro, 1983 Berberis integerrima Berberidaceae D √ Shapiro, 1983 Berberis koreana Berberidaceae D √ Shapiro, 1983 Berberis sieboldii Berberidaceae D √ Shapiro, 1983 Berberis thunbergii Berberidaceae D √ Shapiro, 1983 Berberis vulgaris Berberidaceae D √ Shapiro, 1983 Beta vulgaris Chenopodiaceae D √ √ Granado et al., 1992

Bureau & Bushway, 1986 Bixa orellana Bixaceae D √ Angelucci et al., 1980

Tirimanna, 1981

Blakeslea trispora Choanephoraceae FU √ √ Feofilova & Red'kina, 1975 Feofilova, 1974

Blechnun occidentale Blechnaceae FU √ √ Czeczuga, 1985b Boehmeria nivea Urticaceae D √ √ Santos, 1980 Botrylloides violaceus Styelidae S √ Ookubo & Matsuno, 1985

Matsuno & Sakaguchi, 1984 Botryllus schlosseri Styelidae S √ Ookubo & Matsuno, 1985 Brassica chinensis Brassicaceae D √ Ortaliza, 1969

Species Family Group

Carotene series

Reference α-C β-C γ-C δ-C ε-C

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Carotene series

Brassica napus Brassicaceae D √ √ Joyce, 1954

Brassica oleracea Brassicaceae D √ √ Granado et al., 1992 Bureau & Bushway, 1986 Pospisilova, 1959 Takagi, 1985

Khachik et al., 1999 Wu et al., 1992

Bauer & Demirovska, 1982 Bromelia fastuosa Bromeliaceae M √ √ Bobbio & Scamparini, 1980 Bryocaulon divergens Stereocaulaceae L √ √ Czeczuga & Olech, 1990

Bufo calamita Bufonidae FR √ √ Czeczuga, 1983

Caesalpinia japonica Fabaceae D √ Imamura et al., 1980 Calendula arvensis Asteraceae D √ √ √ √ Baraud, 1958 Calendula officinalis Asteraceae D √ √ √ √ Gusakova, 1983

Zechmeister et al., 1932a Zechmeister et al., 1932b Banaszkiewicz et al., 1963 Goodwin, 1954

Toth & Szabolics,1981 Movchan, 1960 Baszynski, 1954

Camellia sasanqua Theaceae D √ Fishman & Chikovani, 1990a Cantharellus cibarius Cantharellaceae FU √ √ √ Jui et al., 1998

Cantharellus lateritus Cantharellaceae FU √ √ Jui et al., 1998 Cantharellus tabernensis Cantharellaceae FU √ √ √ Jui et al., 1998 Capparis decidua Capparidaceae D √ Gaind et al., 1970 Capparis zeylanica Capparidaceae D √ Laddha & Jolly, 1985 Capsicum annuum Solanaceae D √ √ √ Bureau & Bushway, 1986

Deli et al., 1996 Czinkotai et al., 1989 Biacs et al., 1993 Rodrigues et al.,1988 Mosquera et al., 1992 Mosquera et al., 1994 Mosquera et al., 1993 Gregory et al., 1987

Carcinus maenas Portunidae S √ √ Czeczuga, 1975

Carica papaya Caricaceae D √ √ √ Rao, 1967

Subbarayan & Cama, 1964 Topuriya, 1990

Giri et al., 1980 Yamamoto, 1964 Strocchi et al., 1977 Carthamus tinctorius Asteraceae D √ Baszynski, 1954

Catha edulis Celastraceae D √ Getahun et al., 1973

Cephalotaxus sp Cephalotaxaceae G √ √ Yadav et al., 1987 Cerambyx cerdo Cerambycidae I √ √ Czeczuga, 1988 Ceratodon purpureus Ditrichaceae FE √ Czeczuga, 1980a Ceterach officinarum Aspleniaceae FE √ √ Czeczuga, 1985b Cetraria andrejevii Parmeliaceae L √ √ Czeczuga & Alstrup, 1987 Cetraria cucullata Parmeliaceae L √ √ Czeczuga & Olech, 1990 Cetraria delisei Parmeliaceae L √ √ Czeczuga & Olech, 1990 Czeczuga & Alstrup, 1987 Cetraria islandica Parmeliaceae L √ Czeczuga & Alstrup, 1987 Cetraria nivalis Parmeliaceae L √ √ Czeczuga & Olech, 1990

Czeczuga & Alstrup, 1987 Chattonella japonica Vacuolariaceae A √ Fiksdahl et al., 1984a

Chlamydomonas reinhardti Chlamydomonadaceae A √ Kitayama & Takakura, 1991 Francis et al., 1975 Chlorella fusca Chlorellaceae A √ Burczyk, 1987 Chlorella saccharophila Chlorellaceae A √ Burczyk, 1987

Chlorella sp Chlorellaceae A √ Burczyk, 1987

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Carotene series

Citrus aurantium Rutaceae D √ Toth & Szabolics, 1981

Citrus limon Rutaceae D √ √ Kutateladze, 1974

Citrus paradisi Rutaceae D √ √ √ √ Bureau & Bushway, 1986 Heinonen et al., 1989 Rouseff et al., 1992 Citrus sinensis Rutaceae D √ √ Bureau & Bushway, 1986

Malachi et al., 1974 Shim et al., 1994

Kudritskaya et al., 1983 Cladonia amaurocraea Cladoniaceae L √ √ Czeczuga & Olech, 1990 Cladonia cenotea Cladoniaceae L √ Czeczuga, 1985a Cladonia coccifera Cladoniaceae L √ √ Czeczuga & Olech, 1990

Czeczuga, 1985a Cladonia cornuta Cladoniaceae L √ √ Czeczuga, 1985a Cladonia crispata Cladoniaceae L √ Czeczuga, 1985a Cladonia deformis Cladoniaceae L √ Czeczuga, 1985a Cladonia degenerans Cladoniaceae L √ √ Czeczuga, 1985a Cladonia foliacea Cladoniaceae L √ Czeczuga et al., 1988 Cladonia furcata Cladoniaceae L √ Czeczuga, 1985a Cladonia glauca Cladoniaceae L √ Czeczuga, 1985a Cladonia gracilis Cladoniaceae L √ Czeczuga, 1985a Cladonia impexa Cladoniaceae L √ √ Czeczuga, 1985a Cladonia macilenta Cladoniaceae L √ Czeczuga, 1985a Cladonia mitis Cladoniaceae L √ Czeczuga & Alstrup, 1987 Cladonia nylanderi Cladoniaceae L √ Czeczuga et al., 1988 Cladonia ochrochlora Cladoniaceae L √ Czeczuga, 1985a Cladonia rangiferina Cladoniaceae L √ Czeczuga, 1985a Cladonia scabriuscula Cladoniaceae L √ Czeczuga, 1985a Cladonia sylvatica Cladoniaceae L √ Czeczuga, 1985a Cladonia turgida Cladoniaceae L √ Czeczuga, 1985a Cladonia verticillata Cladoniaceae L √ Czeczuga, 1985a Cochlospermum vitifoleum Cochlospermaceae D √ √ Dixit & Srivastava, 1992a

Colocasia esculenta Araceae M √ Rao, 1967

Coniogramme japonica Pteridaceae FE √ Czeczuga, 1985b Corallina elongata Corallinaceae A √ Palermo et al., 1991 Corallina officinalis Corallinaceae A √ Palermo et al., 1991 Cornicularia divergens Parmeliaceae L √ Czeczuga & Alstrup, 1987 Crambe abyssinica Brassicaceae D √ Baszynski, 1954 Crepis tectorum Asteraceae D √ √ Sergeeva et al., 1984

Crocus sativus Iridaceae M √ √ Duquenois, 1972

Kuhn & Winterstein, 1933 Pfander et al., 1982 Ctenopharyngodon idella Cyprinidae S √ Czeczuga, 1981 Cucumis melo Cucurbitaceae D √ √ √ Bureau & Bushway, 1986

Rojas & Diaz, 1977 Cucumis sativus Cucurbitaceae D √ Granado et al., 1992 Cucurbita maxima Cucurbitaceae D √ Neamtu et al., 1990 Cucurbita moschata Cucurbitaceae D √ Doiiode & Sulledmath, 1986 Cucurbita pepo Cucurbitaceae D √ Granado et al., 1992

Neamtu et al., 1990 Cucurbita sp Cucurbitaceae D √ √ Bureau & Bushway, 1986 Cuscuta australis Convolvulaceae D √ √ Baccarini et al., 1965 Cyclopterus lumpus Cyclopteridae S √ Czeczuga, 1982 Cynara scolymus Asteraceae D √ Granado et al., 1992 Cyrtomium falcatum Dryopteridaceae FE √ √ Czeczuga, 1985b Cystoclonium purpureum Rhodophyllidaceae A √ Findlay & Patil, 1986 Cystopteris bulbifera Dryopteridaceae FE √ Czeczuga, 1985b Cystopteris fragilis Dryopteridaceae FE √ Czeczuga, 1985b

Dactylis glomerata Poaceae M √ Pollard, 1936

Daucus carota Apiaceae D √ √ √ √ Granado et al., 1992 Rao, 1967

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Carotene series

Van Breemen, 1996 Sun, 1994 Sato, 1992 Mok et al., 1976 Czygan & Herboth, 1976 Toth et al., 1995 Koch et al, 1991

Buishand & Gabelman, 1978 Baruffaldi et al., 1981 Sarma & Sarma, 1978 Nishi et al., 1974 Davallia solida Davalliaceae FE √ Czeczuga, 1985b Dermatocarpon miniatum Verrucariaceae L √ Czeczuga & Alstrup, 1987 Desmarestia aculeata Desmarestiaceae A √ Findlay & Patil, 1985 Didemnum moselyi Didemnidae S √ Ookubo & Matsuno, 1985 Dioscorea cayenensis Dioscoreaceae M √ Martin & Ruberte, 1975 Dioscorea versicolor Dioscoreaceae M √ √ Rao, 1967

Diospyros kaki Ebenaceae D √ √ √ √ Fishman & Chikovani, 1990b

Kudritskaya et al., 1984 Ebert & Gross, 1985 Diplazium sibiricum Dryopteridaceae FE √ √ Czeczuga, 1985b Drepanocladus fluitans Amblystegiaceae FE √ Boston et al., 1991 Dryopteris carthusiana Dryopteridaceae FE √ √ Czeczuga, 1985b Dryopteris dilatata Dryopteridaceae FE √ Czeczuga, 1985b Dryopteris filix-mas Dryopteridaceae FE √ Czeczuga, 1985b Dryopteris parasitica Dryopteridaceae FE √ Czeczuga, 1985b Dunaliella bardawil Dunaliellaceae A √ √ Ben-Amotz et al., 1990 Takenaka et al., 1993 Mokady et al., 1989 Dunaliella salina Dunaliellaceae A √ √ Ben-Amotz et al., 1990

Chen et al., 1995 Elaeis guineensis Arecaceae M √ √ √ Mariath et al., 1989

Argoud, 1958

Manorama & Rukmini, 1992 Eleutherococcus koreanus Araliaceae D √ Bladt et al., 1990

Eleutherococcus senticosus Araliaceae D √ Zorikov & Burii, 1974 Equisetum arvensi Equisetaceae FE √ √ Czeczuga, 1985b Equisetum fluviatile Equisetaceae FE √ √ √ Czeczuga, 1985b Equisetum hyemale Equisetaceae FE √ √ Czeczuga, 1985b Equisetum palustre Equisetaceae FE √ Czeczuga, 1985b Equisetum pratense Equisetaceae FE √ Czeczuga, 1985b Equisetum sylvaticum Equisetaceae FE √ √ Czeczuga, 1985b Equisetum telmateia Equisetaceae FE √ √ Czeczuga, 1985b Eriobotrya japonica Rosaceae D √ Ben-Amotz et al., 1990 Erysimum diffusum Brassicaceae D √ Gusakova, 1983 Erythrotrichia carnea Erythropeltidaceae A √ Bjoernland, 1984 Euglena gracilis Euglenaceae A √ √ Gross et al., 1975 Euglena sanguinea Euglenaceae A √ Grung & Jensen, 1993 Fibrocapsa japonica To be determined A √ Fiksdahl et al., 1984a

Ficus carica Moraceae D √ Karag'ozova, 1974

Fontinalis antipyretica Fontinalaceae FE √ √ Czeczuga, 1980a Boston et al., 1991 Fontinalis squamosa Fontinalaceae FE √ √ Czeczuga, 1980a

Fragaria ananassa Rosaceae D √ Gross, 1972

Fragaria sp Rosaceae D √ √ Bureau & Bushway, 1986 Fucus serratus Fucaceae A √ Haugan & Jensen, 1954 Fucus vesiculosus Fucaceae A √ Haugan & Jensen, 1954

Liaaen & Sorensen, 1955 Halsall & Hills, 1971 Funaria hygrometrica Funariaceae FE √ √ Czeczuga, 1980a Fusinus perplexus Fasciolariidae S √ Matsuno & Tsushima, 1989 Galium helderichii Rubiaceae D √ Tzakou et al., 1988

Galium mollugo Rubiaceae D √ Shapiro et al., 1985

Galium tinctorium Rubiaceae D √ Shapiro et al., 1985 Genista dentata Fabaceae D √ √ Schon & Mesqita, 1936 Ginkgo biloba Ginkgoaceae G √ √ √ Yadav et al., 1987

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Carotene series

Glycine max Fabaceae D √ Rao, 1967

Baszynski, 1954 Gnetum africanum Gnetaceae G √ Njoku et al., 1997 Gomphosphaeria aponina Chroococaceae A √ Eng-Wilmont & Martin,

1979

Gonyostomum semen Vacuolariaceae A √ Fiksdahl et al., 1984a Gossypium barbadense Malvaceae D √ Khodzhaev, 1981 Gossypium hirsutum Malvaceae D √ √ Jones, 1979

Hanny & Hedin, 1972

Gossypium sp Malvaceae D √ √ Mc Cormick, 1982

Gracilaria lichenoides Gracilariaceae A √ Aihara & Yamamoto, 1968 Grammatophora oceanica Bacillariophyceae A √ Pennington et al., 1988 Grimmia pulvinata Grimmiaceae FE √ Czeczuga, 1980a Gymnodinium catenatum Gymnodiniaceae A √ Hallegraeff et al., 1991 Gymnogramma sulphurea Pteridaceae FE √ √ Czeczuga, 1985b Gyrodinium aureolum Gymnodiniaceae S √ Tangen & Bjoernland, 1981 Gyrodinium sp Gymnodiniaceae S √ Bjoerland & Tangen, 1979 Haematococcus lacustris Haematococcaceae S √ Donkin, 1976 Halobacterium cutirubrum Halobacteriaceae B √ Kushwaha et al., 1975 Halocynthia roretzi Pyuridae S √ Ookubo & Matsuno, 1985

Matsuno et al., 1984b Hedysarum polybotrys Fabaceae D √ Jiang, 1989 Helianthemum numularum Cistaceae D √ √ Marius et al., 1994 Helianthus annuus Asteraceae D √ Baszynski, 1954

Heliopsis scabra Asteraceae D √ Raszeja & Muszynska, 1980 Heterosigma akashiwo Dinophyceae A √ Fiksdahl et al., 1984b

Hexabranchus sp Hexabranchidae S √ Tanaka et al., 1992 Hibiscus esculentus Malvaceae D √ √ Bureau & Bushway, 1986

Hibiscus sabdariffa Malvaceae D √ Rao, 1967

Hibiscus syriacus Malvaceae D √ √ Hanny & Hedin, 1972 Hanny et al., 1972 Chernenko & Umarov, 1974 Hippophae rhamnoides Elaeagnaceae D √ √ √ Zorikov & Burii, 1974

Sergeeva et al., 1979

Gachechiladze et al., 1981 Lagazidze et al., 1984 Zhmyrko et al., 1978 Hydrilla verticillata Hydrocharitaceae M √ Lin et al., 1979 Hylocomium splendens Hylocomiaceae FE √ Czeczuga, 1980a Hypericum perforatum Clusiaceae D √ √ Omarova et al., 1997

Chaplinskaya, 1956 Hypnum cupressiforme Hypnaceae FE √ √ Czeczuga, 1980a Ianthella basta Ianthellidae S √ Ramdahl et al., 1981 Ianthella flabelliformis Ianthellidae S √ Hertzberg et al., 1989 Ipomoea aquatica Convolvulaceae D √ Ortaliza et al., 1969

Kasemsri et al., 1952 Ipomoea batatas Convolvulaceae D √ √ Bureau & Bushway, 1986

Ortaliza et al., 1969 Iris germanica Iridaceae M √ Buchecker & Jensen, 1975 Iris pseudacorus Iridaceae M √ O'Connor & Drumm, 1941

Jania sp Corallinaceae A √ Palermo et al., 1991

Lactuca sativa Asteraceae D √ √ Granado et al., 1992 Bureau & Bushway, 1986 Laminaria digitata Laminariaceae A √ Haugan & Jensen, 1994 Laminaria saccharina Laminariaceae A √ Haugan & Jensen, 1994

Leptura rubra Cerambycidae I √ Czeczuga, 1988

Lespedeza sp Fabaceae D √ Zorikov & Burii, 1974

Leucobryum glaucum Leucobryaceae FE √ √ Czeczuga, 1980a Ligia exotica Ligiidae S √ Matsuno et al., 1990 Lilium tenuifolium Liliaceae M √ Partali et al., 1987 Lobaria linita Lobariaceae L √ √ Czeczuga & Olech, 1990

Lolium perenne Poaceae M √ Tamas & Popescu, 1985

Lonicera altaica Caprifoliaceae D √ Shapiro et al., 1981 Lonicera caerulea Caprifoliaceae D √ Shapiro et al., 1981 Lonicera edulis Caprifoliaceae D √ Shapiro et al., 1981 Lonicera japonica Caprifoliaceae D √ √ √ Goodwin, 1952

Lota lota Gadidae S √ Czeczuga, 1978

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Carotene series

Lupinus albus Fabaceae D √ El-Fifrawi & Hudson, 1979 Lupinus angustifolius Fabaceae D √ El-Fifrawi & Hudson, 1979 Lupinus luteus Fabaceae D √ El-Fifrawi & Hudson, 1979 Lupinus mutabilis Fabaceae D √ El-Fifrawi & Hudson, 1979 Lycopersicon cheesmanii Solanaceae D √ Chalukova et al., 1985

Lycopersicon esculentum Solanaceae D √ √ Granado et al., 1992 Parry & Horgan, 1992 Laval-Martin et al., 1975 Lycopodium annotinum Lycopodiaceae FE √ Czeczuga, 1985b Lycopodium clavatum Lycopodiaceae FE √ Czeczuga, 1985b Lycopodium complanatum Lycopodiaceae FE √ Czeczuga, 1985 Lycopodium selago Lycopodiaceae FE √ Czeczuga, 1985b Malpighia punicifolia Malpighiaceae D √ √ √ Baraud, 1958 Mangifera indica Anacardiaceae D √ √ √ Meimban et al., 1983

Mercadante et al., 1988b Mantoniella squamata Nephroselmidaceae A √ Egeland et al., 1995 Marchantia polymorpha Marchantiaceae FE √ √ √ Czeczuga, 1980a Matteuccia struthiopteris Dryopteridaceae FE √ √ Czeczuga, 1985b

Bushway et al., 1985 Mauritia vinifera Arecaceae M √ Mariath et al., 1989 Medicago arborea Fabaceae D √ Ignasiak & Lesins, 1975 Medicago cancellata Fabaceae D √ Ignasiak & Lesins, 1975 Medicago carstiensis Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago cretacea Fabaceae D √ Ignasiak & Lesins, 1975 Medicago daghestanica Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago falcata Fabaceae D √ Ignasiak & Lesins, 1975 Medicago glomerata Fabaceae D √ Ignasiak & Lesins, 1975 Medicago glutinosa Fabaceae D √ Ignasiak & Lesins, 1975 Medicago hemicycla Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago hybrida Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago leiocarpa Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago marina Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago papillosa Fabaceae D √ Ignasiak & Lesins, 1975 Medicago pironae Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago platycarpos Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago prostrata Fabaceae D √ Ignasiak & Lesins, 1975 Medicago rhodopea Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago rupestris Fabaceae D √ Ignasiak & Lesins, 1975 Medicago ruthenica Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago sativa Fabaceae D √ Toth et al., 1995

Ignasiak & Lesins, 1975 Medicago saxatilis Fabaceae D √ √ Ignasiak & Lesins, 1975 Medicago suffruticosa Fabaceae D √ √ Ignasiak & Lesins, 1975 Melinis minutiflora Poaceae M √ Calle Alvarez et al., 1986 Metasequoia glyptosboides Taxodiaceae G √ √ √ Czeczuga, 1987 Microlepia speluncae Dennstaedtiaceae FE √ √ Czeczuga, 1985b Millingtonia hortensis Bignoniaceae D √ Mangayarkarasi et al.,1984 Mimosa biuncifera Fabaceae D √ Kudritskaya et al., 1988a Mimulus cupreus Scrophulariaceae D √ Goodwin & Thomas, 1964 Mimulus tigrinus Scrophulariaceae D √ Goodwin & Thomas, 1964

Mnium affine Mniaceae FE √ √ Czeczuga, 1980a

Mnium cuspidatum Mniaceae FE √ √ Czeczuga, 1980a Mnium undulatum Mniaceae FE √ √ Czeczuga, 1980a Momordica charantia Cucurbitaceae D √ √ √ Rodriguez et al., 1976 Monarda didyma Lamiaceae D √ Brieskorn & Meister, 1965 Monochamus pistor Cerambycidae I √ Czeczuga, 1988 Montanoa karwinski Asteraceae D √ Quijano et al., 1995 Morinda citrifolia Rubiaceae D √ Aalbersberg et al., 1993 Moringa pterygosperma Moringaceae D √ Ortaliza et al., 1969

Morus alba Moraceae D √ Yen et al., 1996

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Carotene series

Nephroma laevigatum Peltigeraceae L √ Czeczuga et al., 1988 Nephroma parile Peltigeraceae L √ Czeczuga & Alstrup, 1987 Nicotiana plumbaginifolia Solanaceae D √ Parry & Horgan, 1992 Nicotiana tabacum Solanaceae D √ Lichtenthaler et al., 1975 Nitzschia sp Nitzschiaceae A √ Pennington et al., 1988

Ocimum sanctum Lamiaceae D √ Skaltsa et al., 1987

Odontoschisma denudatum Odontoschismaceae FE √ √ Czeczuga, 1980a Olea europaea Oleaceae D √ √ √ Golubev et al., 1986 Onoclea sensibilis Dryopteridaceae FE √ Czeczuga,1985b Orthosiphon grandiflorus Lamiaceae D √ √ Kudritskaya et al., 1988b Orychophragmus violaceus Brassicaceae D √ Li et al., 1997 Oscillatoria agardhii Oscillatoriaceae A √ Ronneberg et al., 1980

Foss et al., 1986 Oscillatoria bornetii Oscillatoriaceae A √ Foss et al., 1986 Oscillatoria limosa Oscillatoriaceae A √ Foss et al., 1986 Francis et al., 1970 Oscillatoria rubescens Oscillatoriaceae A √ Ronneberg et al., 1980

Paralithodes brevipes Lithodidae S √ Matsuno Maoka, 1988 Parmelia acetabulum Parmeliaceae L √ Czeczuga et al., 1989 Passiflora edulis Passifloraceae D √ √ Mercadante et al., 1998a Pellaea rotundifolia Pteridaceae FE √ Czeczuga, 1985b Pellia endiviaefolia Pelliaceae FE √ Asakawa & Takemoto, 1978 Pellia fabbroniana Pelliaceae FE √ Czeczuga, 1980a Peltigera aphthosa Peltigeraceae L √ √ Czeczuga, 1986

Czeczuga, 1980b Peltigera canina Peltigeraceae L √ Czeczuga, 1980b Peltigera erumphens Peltigeraceae L √ Czeczuga, 1980b Peltigera hazszlynskyi Peltigeraceae L √ √ Czeczuga, 1980b

Peltigera leucophlebia Peltigeraceae L √ Czeczuga & Olech, 1990 Czeczuga, 1980b Peltigera malacea Peltigeraceae L √ √ Czeczuga & Olech, 1990

Czeczuga, 1980b Peltigera polydactyla Peltigeraceae L √ Czeczuga, 1980b Peltigera ponojensis Peltigeraceae L √ Czeczuga et al., 1989 Peltigera praetexta Peltigeraceae L √ √ √ Czeczuga, 1980b

Peltigera rufescens Peltigeraceae L √ Czeczuga & Alstrup, 1987 Czeczuga, 1980b Pelvetia canaliculata Fucaceae A √ Haugan & Jensen, 1954 Penaeus japonicus Penaeidae S √ Katagiri et al., 1987 Persea americana Lauraceae D √ √ √ Gross et al., 1972

Petroselinum crispum Apiaceae D √ Francis & Isaken, 1989 Phaeocystis sp Chrysocapsaceae S √ Bjornland et al., 1988 Phaffia rhodozyma Hyphomycetes FU √ Yajima et al., 1993 Phaseolus vulgaris Fabaceae D √ √ Granado et al., 1992

Rao, 1967

Parry & Horgan, 1992 Bureau & Bushway, 1986 Wu et al., 1992 Lopez-Hernandez et al.,

1993

Phegopteris dryopteris Thelypteridaceae FE √ Czeczuga, 1985b Pheodactylum tricornutum To be determined A √ Pennington et al., 1988 Phormidium laminosum Oscillatoriaceae A √ Fresnedo et al., 1991 Phycomyces blakesleeanus Mucoraceae FU √ √ Bramley & Davies, 1975

Bramley & Davies, 1976 Elahi et al., 1975 Eslava et al., 1974 Desai et al., 1975 Lee et al., 1975 Physalis alkekengi Solanaceae D √ √ Baraud, 1958 Physconia pulverulacea Physciaceae L √ √ Czeczuga, 1986 Picea abies Pinaceae G √ √ √ Pfeifhofer & Grill, 1984

Grill et al., 1984 Hoque, 1988

Pinus massoniana Pinaceae G √ Zhou et al., 1984

Pinus roxburghii Pinaceae G √ Yadav et al., 1987

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Carotene series

Pisum sativum Fabaceae D √ √ Parry & Horgan, 1992 Bureau & Bushway, 1986 Pleurozia schreberi Pleuroziaceae FE √ Czeczuga, 1980a Plumbago zeylanica Plumbaginaceae D √ Heble, 1977

Polycitor proliferus Polycitoridae S √ Ookubo & Matsuno, 1985 Polystichum tsus- sinense Dryopteridaceae FE √ Czeczuga, 1985b Polytrichum commune Polytrichaceae FE √ √ Czeczuga, 1980a Polytrichum formosum Polytrichaceae FE √ √ Czeczuga, 1980a Polytrichum gracile Polytrichaceae FE √ Czeczuga, 1980a Polytrichum juniperinum Polytrichaceae FE √ Czeczuga, 1980a Polytrichum piliferum Polytrichaceae FE √ √ Czeczuga, 1980a

Porphyra tenera Bangiaceae A √ Okai et al., 1996

Portulaca oleracea Portulacaceae D √ Simopoulos et al., 1992 Potentilla argentea Rosaceae D √ √ Goncharov & Kotov, 1992 Potentilla erecta Rosaceae D √ √ Goncharov & Kotov, 1992 Protula tubularia Serpulidae S √ √ Czeczuga, 1984 Prunus armeniaca Rosaceae D √ √ Bureau & Bushway, 1986

Prunus avium Rosaceae D √ Gross, 1985

Prunus domestica Rosaceae D √ Heinonen et al., 1989

Prunus padus Rosaceae D √ Zorikov & Burii, 1974

Prunus persica Rosaceae D √ √ Bureau & Bushway, 1986 Mc Carty & Lesley, 1954 Molnar et al., 1987 Pseudoscourfieldia marina Prasinophyceae A √ Egeland et al., 1995 Pteridium aquilinum Dennstaedtiaceae FE √ √ Czeczuga, 1985b Ptilium crista-castrensis Hypneaceae FE √ √ Czeczuga, 1980a Pulicaria paludosa Asteraceae D √ Diaz et al., 1988

Pyracantha sp Rosaceae D √ Wang et al., 1992

Pyramimonas parkeae Pyramimonadaceae A √ Sasa et al., 1992 Ramalina capitata Ramalinaceae L √ Hoyos & Manrique, 1995 Ranunculus ficaria Ranunculaceae D √ Cameroni & Bernabei, 1957 Raphanus sativus Brassicaceae D √ Becker & Lichtenthaler,

1975

Renealmia alpinia Zingiberaceae M √ Lognay et al., 1991 Rhaponticum carthamoides Asteraceae D √ Gusakova, 1983 Rhododendron ellipticum Ericaceae D √ Ho & Lin, 1995 Rhodomicrobium vannielii Rhodospirillaceae B √ Britton et al., 1995 Rhodotorula glutinis Hyphomycetes FU √ Hayman et al., 1974

Rhodotorula mucilaginosa Hyphomycetes FU √ √ Margalith & Meydav, 1968 Rhodotorula rubra Hyphomycetes FU √ Shih & Hang, 1996

Riccardia sinuata Aneuraceae FE √ Benesova et al., 1969 Riccia fluitans Ricciaceae FE √ √ Czeczuga, 1980a Ricinus communis Euphorbiaceae D √ Baszynski, 1954 Rivina humilis Phytolaccaceae D √ Lopez, 1982

Rosa canina Rosaceae D √ Razungles et al., 1989

Hodisan et al., 1997

Rosa foetida Rosaceae D √ Marki-Fische et al., 1984

Rosa pomifera Rosaceae D √ Marki-Fischer et al., 1983 Rosa rugosa Rosaceae D √ Razungles et al., 1989

Rosa sp Rosaceae D √ Williams & Goodwin, 1965

Rubus idaeus Rosaceae D √ √ Bureau & Bushway, 1986

Rumex vesicarius Polygonaceae D √ Rao, 1967

Salvia arisanensis Lamiaceae D √ Wu & Huang, 1975 Salvia hayatana Lamiaceae D √ Wu & Huang, 1975 Salvia hualiensis Lamiaceae D √ Wu & Huang, 1975 Salvia keitaoensis Lamiaceae D √ Wu & Huang, 1975 Salvia scapiformis Lamiaceae D √ Wu & Huang, 1975 Sandersonia aurantiaca Liliaceae M √ Lewis et al., 1998 Sansevieria cylindrica Agavaceae M √ Moustafa et al., 1986 Sarcopoterium spinosum Rosaceae D √ Vitsaropoulou et al., 1981 Scenedesmus obliquus Scenedesmaceae A √ Burczyk, 1987

Scenedesmus quadricauda Scenedesmaceae A √ Burczyk, 1987 Sesbania grandiflora Fabaceae D √ Andal & Sulochana, 1986 Skeletonema costatum Coscinodiscaceae A √ Pennington et al., 1988 Skeletonema menzelii Coscinodiscaceae A √ Pennington et al., 1988

Smilax sp Liliaceae M √ Kudritskaya et al., 1982

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Carotene series

Munteanu et al., 1980 Solanum nigrum Solanaceae D √ Dan et al., 1982 Solanum persicum Solanaceae D √ √ Novruzov, 1983 Solanum tuberosum Solanaceae D √ √ Granado et al., 1992 Solorina crocea Peltigeraceae L √ Czeczuga & Olech, 1990 Sorbus aucuparia Rosaceae D √ √ Valadon et al., 1972 Sphaerophorus globosus Sphaerophoraceae L √ Czeczuga & Olech, 1990 Sphagnum apiculatum Sphagnaceae FE √ √ Czeczuga, 1980a Sphagnum magellanicum Sphagnaceae FE √ √ Czeczuga, 1980 Sphagnum palustre Sphagnaceae FE √ √ √ Czeczuga, 1985b Sphagnum recurvum Sphagnaceae FE √ √ √ Czeczuga, 1985b Sphagnum squarrosum Sphagnaceae FE √ √ √ Czeczuga, 1985b Spinacia oleracea Chenopodiaceae D √ √ Granado et al., 1992

Rao, 1967

Bureau & Bushway, 1986 Spirulina dunaliella Oscillatoriaceae A √ Jenkins et al., 1993

Spirulina sp Oscillatoriaceae A √ Schwartz et al., 1988 Sporobolomyces chosaticus Hyphomycetes FU √ Golyakov & Tikhonova,

1975

Sporobolomyces paraseus Hyphomycetes FU √ Golyakov & Tikhonova, 1975

Sporobolomyces roseus Hyphomycetes FU √ Golyakov & Tikhonova, 1975

Staphylococcus aureus Micrococcaceae B √ √ Mel'nikova & Ignatov, 1973 Czecuga & Heczko, 1988 Stemmadenia glabra Apocynaceae D √ Ciccio et al., 1982

Stereocaulon alpinum Stereocaulaceae L √ √ Czeczuga & Olech, 1990 Czeczuga & Alstrup, 1987 Czeczuga, 1986 Stereocaulon paschale Stereocaulaceae L √ Czeczuga & Alstrup, 1987 Stereocaulon vesuvianum Stereocaulaceae L √ √ Czeczuga & Olech, 1990

Czeczuga et al., 1989 Stereocaulon vulcani Stereocaulaceae L √ Czeczuga et al., 1988 Stevia rebaudiana Asteraceae D √ Cheng & Chang, 1983 Stichopus regalis Stichopodidae S √ Czeczuga, 1984 Sticta canariensis Lobariaceae L √ Czeczuga et al., 1988 Styela clava Styelidae S √ Ookubo & Matsuno, 1985 Styela plicata Styelidae S √ Ookubo & Matsuno, 1985 Suberites sericeus Suberitidae S √ Matsuno et al., 1984a Symphytum officinale Boraginaceae D √ Fukumoto & Kuwano, 1975

Tagetes erecta Asteraceae D √ Khachik et al., 1999

Tamus communis Dioscoreaceae M √ √ √ Baraud, 1958

Tanacetum vulgare Asteraceae D √ Banthorpem & Justice, 1972 Taraxacum officinale Asteraceae D √ Booth, 1964

Tecoma argentea Bignoniaceae D √ Dixit & Srivastava, 1992b

Tethya aurantia Clionidae S √ √ √ Czeczuga, 1984

Tetragonia tetragonoides Aizoaceae D √ Lee, 1975 Tetraselmis sp Chlamydomonadaceae A √ Egeland et al., 1995 Tetraselmis wettsteinii Chlamydomonadaceae A √ Egeland et al., 1995 Thalassiosira eccentrica Thalassiosiraceae A √ Pennington et al., 1988 Thalassiosira oceanica Thalassiosiraceae A √ Pennington et al., 1988 Thalassiosira pseudonana Thalassiosiraceae A √ Pennington et al., 1988 Thalassiosira rotula Thalassiosiraceae A √ Pennington et al., 1988 Thamnolia vernicularis Siphulaceae L √ Czeczuga & Olech, 1990 Thelypteris palustris Thelypteridaceae FE √ Czeczuga, 1985b

Thespesia populnea Malvaceae D √ Datta, 1968

Thorascophaera heimii Coccolithophycidae S √ Bjornland, 1990 Trichosanthes cucumeroide Cucurbitaceae D √ √ Matsuno & Nagata, 1971

Matsuno et al., 1970 Trifolium repens Fabaceae D √ √ Sergeeva et al., 1984 Trigonella foenum-gracum Fabaceae D √ Rao, 1967

Triticum durum Poaceae M √ Lier, 1975

Ulex europaeus Fabaceae D √ √ Schon, 1936

Ulex gallii Fabaceae D √ √ Schon, 1936

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Carotene series

Undaria pinnatifida Alariaceae A √ Okuda & Ukegawa, 1977 Urtica dioica Urticaceae D √ Kudritsata et al., 1987 Usnea glabrata Parmeliaceae L √ √ Czeczuga et al., 1989 Usnea sulphurea Parmeliaceae L √ Czeczuga & Olech, 1990 Vaccinium corymbosum Ericaceae D √ √ Bureau & Bushway, 1986 Vaccinium macrocarpon Ericaceae D √ √ Heinonen et al., 1989 Vacuolaria virescens Vacuolariaceae A √ Fiksdahl et al., 1984a Verbena officinalis Verbenaceae D √ Winde et al., 1961 Vernonia baccharoides Asteraceae D √ Ugaz & Fort, 1984 Verticillium agaricinum Hyphomycetes FU √ Valadon & Mummery, 1974 Viburnum opulus Caprifoliaceae D √ Shapiro et al., 1992 Viscum album Loranthaceae D √ Neamtu & Bodea, 1970

Cornelia & Stirban, 1976 Vitis vinifera Vitaceae D √ √ √ Heinonen et al., 1989

Zherebin & Kolesnik, 1984

Zea mays Poaceae M √ Rao, 1967

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